Introduction to the analysis of maternal mortality
Maternal mortality has long been a focus of national health services, but its salience has increased over the last two decades with the establishment of quantitative goals. During that time, the international community has periodically established targets for the reduction of maternal mortality, measured as the Maternal Mortality Ratio (MMR), maternal deaths per 100,000 live births. The World Summit for Children in 1990 set the goal of reducing MMR by half between 1990 and 2000. The 1994 International Conference on Population and Development (ICPD) reiterated this goal, but set the additional longer-term target of reducing the rate by a further half by 2015. The Millennium Summit in 2000 adopted the ICPD target for the fifth MDG (the improvement of maternal health). The target was thus to reduce the MMR by three-quarters between 1990 and 2015. The 2011 report of the Commission on Information and Accountability for Women’s and Children’s Health, established by the Secretary-General of the United Nations, reaffirmed the importance of timely reporting on MMR as one of 11 indicators of maternal, newborn, and child health. It is thus clear that the measurement of maternal mortality has a very high priority. This section discusses broad options for such measurement.
The International Classification of Diseases Revision 10 (ICD-10) defines a maternal death as follows. "A maternal death is defined as the death of a woman while pregnant or within 42 days of termination of pregnancy, irrespective of the duration and site of the pregnancy, from any cause related to or aggravated by the pregnancy or its management but not from accidental or incidental causes." Measuring maternal deaths thus involves the determination of cause of death, an issue not addressed elsewhere in this manual. Maternal deaths are divided into direct obstetric deaths (of which the major specific causes are haemorrhage, obstructed labour, eclampsia, sepsis and consequences of abortion) and indirect obstetric deaths (pregnancy-related deaths among women with a pre-existing or newly developed health problem exacerbated by the pregnancy or delivery).
The measurement of maternal mortality represents a major problem for countries lacking largely complete birth and death registration (Graham, Ahmed, Stanton et al. 2008) not only because deaths are not recorded but also because of the need to ascertain cause of death (see for example Mathers, Fat, Inoue et al. (2005)). Cause of death is best determined by a physician present close to the time of death, but many deaths occur without the presence of a doctor. Further, even when a doctor does certify the death, deaths that occur outside of the labour ward may be incorrectly ascribed to a non-maternal cause. Some progress has been made in recent years with the development and application of verbal autopsy methods, whereby family members are asked to report signs and symptoms surrounding the death, but there is still considerable controversy about how well such methods work (Chandramohan, Rodrigues, Maude et al. 1998). The description of verbal autopsy instruments and analysis is beyond the scope of this Manual.
In part because of the difficulty of identifying true maternal deaths, ICD-10 also defines a pregnancy-related death as one that occurs during pregnancy, delivery or the 42 days after the end of the pregnancy, regardless of cause of death. The category pregnancy-related death thus includes all maternal deaths plus the accidental or incidental deaths excluded from the category “maternal”. The advantage of the pregnancy-related category is that it appears to be easier to implement; it only requires information on the timing of death relative to a pregnancy, without specific knowledge of true cause of death. The disadvantages are that measures of pregnancy-related mortality are frequently misinterpreted as measures of maternal mortality, and that any trend in pregnancy-related mortality not due to maternal causes will limit the value of the measure for tracking impact of maternal health interventions. Demographic surveys generally measure pregnancy-related deaths and avoid the necessity for cause ascertainment.
There is active debate, and no consensus, as to the relationship that exists in practice between a reported number of pregnancy-related deaths and some unknown true number of maternal deaths. Clearly by definition the true number of pregnancy-related deaths has to be the same as, or larger than, the true number of maternal deaths, since all maternal deaths are pregnancy-related, but not all pregnancy-related deaths are maternal. In practice, however, the situation is less clear-cut because of possible reporting errors. There are those who argue that reported pregnancy-related deaths exceed true maternal deaths (Garenne, McCaa and Nacro 2008; Stecklov 1995) whereas others argue that pregnancy-related deaths are likely to be under-reported because, for example, a respondent may not have known that the deceased was pregnant at the time of death (Shahidullah 1995; Wilmoth 2009). The relationship could, therefore, go either way. This manual does not come down firmly in support of either of these views, but instead emphasizes that good practice requires that measures be labelled correctly. Thus a measure based on reported pregnancy-related deaths should be reported as a measure of pregnancy-related mortality, whereas a measure based on what are thought to be true maternal deaths (identified by a verbal autopsy for example) should be reported as a measure of maternal mortality.
Basic measures of maternal mortality
There are two common measures of maternal mortality (and corresponding measures for pregnancy-related mortality). They are the Maternal Mortality Ratio (MMR), the target for MDG-5, and the Maternal Mortality Rate (here abbreviated as MMRate). There are two other measures that will often be encountered: the proportion of deaths of women of reproductive age that are maternal (often abbreviated as PMDF), and the lifetime risk of dying a maternal death (LTR). The latter measure is used primarily for advocacy purposes.
Maternal Mortality Ratio
The MMR is the number of maternal deaths in a period per 100,000 live births in the same period. Note the use of live births rather than pregnancies in the denominator. The MMR is primarily a measure of obstetric risk, roughly the risk of dying per 100,000 risky events.
Maternal Mortality Rate
The MMRate is a cause-specific mortality rate. It is the number of maternal deaths in a period per 1,000 person-years lived by the female population of reproductive age (usually ages 15-49).
The MMR and MMRate share a numerator, and have a simple relationship to one another:
where, for a given time period, MD is maternal deaths, LB is live births, FPRA is the person-years lived by the female population of reproductive age, and GFR is the General Fertility Rate expressed per 1,000 women of reproductive age.
Proportion Maternal of Deaths of Women of Reproductive Age
The PMDF is MD/FDRA, where FDRA is the number of deaths of women of reproductive age. It is used primarily in modeling exercises (for example, Hill, Thomas, AbouZahr et al. (2007), Hogan, Foreman, Naghavi et al. (2010), Wilmoth, Zureick, Mizoguchi et al. (2010) and Wilmoth, Mizoguchi, Oestergaard et al. (2012)) but is also of some value for data quality assessment (see below).
The LTR is usually implemented as the risk of dying from a maternal cause from age 15 onwards. Wilmoth (2009) suggests calculating the measure per 1,000 women reaching age 15; i.e., as
where T15 and T50 are the person-years lived above ages 15 and 50 respectively, and l15 is the survivors to age 15, in an appropriate life table for the population in question.
Each of the four measures above has a pregnancy-related corollary, calculated by replacing maternal deaths by pregnancy-related deaths.
Other than civil registration, there are two widely used approaches to the collection of data needed to measure pregnancy-related mortality: the full sibling history (FSH); and a large household survey or census that collects data on recent household deaths (HSHD). The summary sibling history (Graham, Brass and Snow 1989) is now rarely used, partly because it produces estimates that represent averages over very long time frames.
The full sibling history
A full sibling history (FSH) involves complex and detailed data collection, requiring very careful training and supervision of field staff to be executed correctly. It is therefore not an appropriate methodology to include in a census. The FSH has been widely included as the “Maternal Mortality Module” in DHSs since 1991, and has also been included in some other household surveys. The FSH collects information from eligible respondents. In most DHSs, women eligible for the birth history are also those eligible for the FSH, but some surveys have also collected FSHs from eligible male respondents. Information is collected about all brothers and sisters born to the same mother. The FSH can thus be thought of as the respondent’s mother’s full birth history, excluding the respondent herself (or himself). In the DHS, the information collected about each sibling is: name; sex; whether still alive; if still alive, age in years; if dead, how many years ago did the sibling die and how old was he or she at death. For deaths of women of reproductive age, additional questions enquire whether the sister died (i) while pregnant; (ii) during childbirth; or (iii) within 42 days or 2 months of the end of a pregnancy.
It will be clear from the above that measures calculated from an FSH are of pregnancy-related mortality, not maternal mortality. The sibling history does not lend itself to the application of a verbal autopsy (which would be necessary for calculating maternal mortality), because a sister of reproductive age reported to have died may well have died in a different household than the respondent, who thus may have little direct knowledge of signs and symptoms preceding the death. It is generally not feasible to try to identify the household where the death occurred and conduct a verbal autopsy with a member of that household.
The FSH provides information on pregnancy-related deaths and female exposure, and thus a basis for estimating pregnancy-related mortality rates. If pregnancy-related mortality ratios (PRMRs) are to be calculated, information must also be available on live births. A typical DHS collects a full birth history (FBH) as well as an FSH, so this is usually not a problem.
The summary sibling history
The use of information on sibling survival to estimate maternal mortality was first proposed by Graham, Brass and Snow (1989). They proposed using a summary sibling history. Such a summary history collects information by sex on the aggregate number of siblings the respondent had, the number who survived to age 15 (or first marriage), and – for sisters who died after age 15 – whether they were pregnant, in childbirth, or in the 42 days post-partum when they died. This method is not recommended for use. The sisters of a respondent can differ in age from the respondent herself by plus or minus 30 years, with the result that the deaths of sisters can be spread over a very long time period prior to a survey. Reference dates of maternal mortality estimates derived from summary sibling histories are thus located well in the past (on average as much as 12 years before the survey), making them of limited practical value. As a consequence the method will not be described further.
The census or large household survey collecting data on recent household deaths
Censuses in the 1970s and 1980s in countries lacking complete civil registration often collected information on recent household deaths, usually those that occurred in the last 12 months. Concerns about data quality limited the use of such questions in the 1990 and 2000 rounds of censuses, but renewed interest in adult mortality and specifically in maternal mortality led to a sharp increase in their use in the 2010 round. A common format for such questions is to ask whether any usual household member died in the preceding 12 months (sometimes the question refers to a different period such as the time since a fixed date or memorable event). If the answer is yes, the deceased’s name, sex and age at death are recorded. If the death is of a woman of reproductive age, an additional question or questions about the timing of death relative to pregnancy are asked, namely did the deceased die while pregnant, during delivery, or in the 6 weeks (sometimes 2 months) after the end of the pregnancy? The methodology is reviewed by Stanton, Hobcraft, Hill et al. (2001), and experience with it is reviewed by Hill, Queiroz, Stanton et al. (2007) and Hill, Queiroz, Wong et al. (2009).
As generally used, these questions on recent deaths identify pregnancy-related deaths. However, some attempts have been made to follow up reported deaths of women of reproductive age (or a sample of such deaths) with a verbal autopsy to identify true maternal deaths. This has been done in a number of very large household sample surveys (e.g. in the Bangladesh Maternal Morbidity and Mortality Survey 2001 (Hill, El-Arifeen, Koenig et al. 2006), but also following at least two censuses (1986 in Iran and 2007 in Mozambique).
A census or large household survey that collects information on recent household deaths will always record a household roster by age and sex. This roster provides information on denominators for pregnancy-related mortality rates (PRMRates). Additional information on recent fertility will be needed to calculate PRMRates. This will usually be collected in the form of a question for women of reproductive age as to whether they had a live birth in the year before the survey or a question on the date of each woman’s most recent live birth. Information on life-time fertility should also be collected to permit the evaluation and possible adjustment of the data on fertility (see the section on fertility estimation using a relational Gompertz model).
Data collected at health facilities
A major expense of household surveys is the cost of getting an interviewer to the (correct) household. Much of this expense can be eliminated by taking advantage of respondents coming to the interviewer, such as to give birth in a health facility. Health facilities are also likely to record births and deaths and cause of death that occur at the facility as part of a routine health management information system. However, the problem with such data is selection bias: we can never be sure that the women who give birth in a facility are representative of all mothers. To improve coverage, experiments are being conducted to find out whether health extension workers or the equivalent working in communities can collect adequate data on births and deaths. Such an approach is akin to a sample registration system.
An analysis strategy for facility data has been proposed but not implemented. Starting with the assumption that women who deliver in a health facility (or visit a health facility for some other pregnancy-related condition) are a biased sample of all mothers (it is not clear which way the bias will run, whether women having fewer pregnancy-related health issues or those having more will predominate), if one could estimate the selection probabilities correctly, the statistics collected could be adjusted for bias. For example, women on visiting a health facility could be asked their age, children ever born and children still alive, plus a number of additional questions about their socio-economic condition. The children ever born and children still alive could then be modelled onto the socio-economic structure of the whole population, available for example from a population census. To our knowledge, this approach has never been tested.
Chandramohan D, LC Rodrigues, GH Maude and RJ Hayes. 1998. "The validity of verbal autopsies for assessing the causes of institutional maternal death", Studies in Family Planning 29(4):414-422. doi: http://dx.doi.org/10.2307/172253
Garenne M, R McCaa and K Nacro. 2008. "Maternal mortality in South Africa in 2001: From demographic census to epidemiological investigation", Population Health Metrics 6:4. doi: http://dx.doi.org/10.1186/1478-7954-6-4
Graham W, S Ahmed, C Stanton, C Abou-Zahr and O Campbell. 2008. "Measuring maternal mortality: An overview of opportunities and options for developing countries", BMC Medicine 6:12. doi: http://dx.doi.org/10.1186/1741-7015-6-12
Graham W, W Brass and RW Snow. 1989. "Estimating maternal mortality: The sisterhood method", Studies in Family Planning 20(3):125-135. doi: http://dx.doi.org/doi:10.2307/1966567
Hill K, S El-Arifeen, M Koenig, A Al-Sabir, K Jamil and H Raggers. 2006. "How should we measure maternal mortality in the developing world? A comparison of household deaths and sibling history approaches", Bulletin of the World Health Organization 84(3):173-180. doi: http://dx.doi.org/10.2471/BLT.05.027714
Hill K, BL Queiroz, C Stanton and C AbouZahr. 2007. "Measuring maternal mortality via the population census: Experience from Africa," Paper presented at 5th African Population Conference. Arusha, Tanzania, 10-14 December 2007.
Hill K, BL Queiroz, L Wong, J Plata et al. 2009. "Estimating pregnancy-related mortality from census data: Experience in Latin America", Bulletin of the World Health Organization 87(4):288-295. doi: http://dx.doi.org/10.2471/BLT.08.052233
Hill K, K Thomas, C AbouZahr, N Walker et al. 2007. "Estimates of maternal mortality worldwide between 1990 and 2005: An assessment of available data", The Lancet 370(9595):1311-1319. doi: http://dx.doi.org/10.1016/S0140-6736(07)61572-4
Hogan MC, KJ Foreman, M Naghavi, SY Ahn et al. 2010. "Maternal mortality for 181 countries, 1980-2008: A systematic analysis of progress towards Millennium Development Goal 5", The Lancet 375(9726):1609-1623. doi: http://dx.doi.org/10.1016/S0140-6736(10)60518-1
Mathers CD, DM Fat, M Inoue, C Rao and AD Lopez. 2005. "Counting the dead and what they died from: An assessment of the global status of cause of death data", Bulletin of the World Health Organization 83(3):171-177.
Shahidullah M. 1995. "The sisterhood method of estimating maternal mortality: The Matlab experience", Studies in Family Planning 26(2):101-106. doi: http://dx.doi.org/10.2307/2137935
Stanton C, J Hobcraft, K Hill, N Kodjogbé et al. 2001. "Every death counts: Measurement of maternal mortality via a census", Bulletin of the World Health Organization 79(7):657-664.
Stecklov G. 1995. "Maternal mortality estimation: Separating pregnancy-related and non-pregnancy-related risks", Studies in Family Planning 26(1):33-38. doi: http://dx.doi.org/10.2307/2138049
Wilmoth J, S Zureick, N Mizoguchi, M Inoue and M Oestergaard. 2010. Levels and Trends of Maternal Mortality in the World: The Development of New Estimates by the United Nations. Geneva: WHO, UNICEF, UNFPA and the World Bank. http://www.who.int/reproductivehealth/publications/monitoring/MMR_technical_report.pdf
Wilmoth JR. 2009. "The lifetime risk of maternal mortality: Concept and measurement", Bulletin of the World Health Organization 87(4):256-262. doi: http://dx.doi.org/10.2471/BLT.07.048280
Wilmoth JR, N Mizoguchi, MZ Oestergaard, L Say et al. 2012. "A new method for deriving global estimates of maternal mortality", Statistics, Politics, and Policy 3(2):Article 3. doi: http://dx.doi.org/10.1515/2151-7509.1038